Breed differences in domestic dogs' (Canis familiaris) - Evolutionary ...

Breed differences in domestic dogs’ (Canis familiaris) comprehension of human communicative signals Victoria Wobber1,2 Brian Hare2,3 Janice Koler-Matznick4 Richard Wrangham1 and Michael Tomasello2

(1) Department of Anthropology, Harvard University, Cambridge, MA 02138, U.S.A. / (2) Max Planck Institute for Evolutionary Anthropology, Leipzig, D-04103, Germany / (3) Department of Evolutionary Anthropology, Duke University, Durham, NC 27705 U.S.A. / (4) New Guinea Singing Dog Conservation Society, Central Point, OR 97502, U.S.A.

Recent research suggests that some human-like social skills evolved in dogs (Canis familiaris) during domestication as an incidental by-product of selection for “tame” forms of behavior. It is still possible, however, that the social skills of certain dog breeds came under direct selection that led to further increases in social problem solving ability. To test this hypothesis, different breeds of domestic dogs were compared for their ability to use various human communicative behaviors to find hidden food. We found that even primitive breeds with little human contact were able to use communicative cues. Further, “working” dogs (shepherds and huskies: thought to be bred intentionally to respond to human cooperative communicative signals) were more skilled at using gestural cues than were non-working breeds (basenji and toy poodles: not thought to have been bred for their cooperative-communicative ability). This difference in performance existed regardless of whether the working breeds were more or less genetically wolf-like. These results suggest that subsequent to initial domesticating selection giving rise to cue-following skills, additional selection on communicative abilities in certain breeds has produced substantive differences in those breeds’ abilities to follow cues. Keywords: dogs, social cognition, evolution, breed differences, domestication

Domestic dogs are unusually skilled at reading human social and communicative behaviors when compared to other non-humans (Cooper et al 2003, Hare and Tomasello 2005, Miklosi et al 2005). Dogs have been shown to spontaneously use Interaction Studies 10:2 (2009), 206–224. doi 10.1075/is.10.2.06wob issn 1572–0373 / e-issn 1572–0381 © John Benjamins Publishing Company

Breed differences in cue-following 207

a number of communicative cues (e.g. a pointing gesture or gaze), including completely novel behaviors, to find hidden food (Agnetta et al 2000, Hare and Tomasello 1999, Miklosi, 2008, Miklosi et al 1998, Riedel et al 2006, Soproni et al 2001, 2002). When directly compared on the same tasks, dogs are even more skillful at using human social cues than chimpanzees and wolves — though human-reared wolves are able to use such cues (Hare et al 2002, Miklosi et al 2003, Viranyi et al 2008). Although wolves can be trained to use these cues, this is also the case for many non-human primate species — however, it seems unlikely that either wolves or non-human primates show as extensive flexibility in interpreting these cooperative signals as do domestic dogs (Udell et al, 2008). Studies of dog puppies of various ages and rearing histories suggest that these abilities do not require extensive exposure to humans in order to develop (Hare et al 2002, Riedel et al 2008). Further, fox kits experimentally selected only to approach a human without fear or aggression were as skillful as age matched dog puppies at using a human pointing gesture. Importantly, the kits from the selected population were more skillful than foxes from a control population (i.e. not selected based on their approach behavior towards humans) (Hare et al 2005). These results suggest that the foxes not only evolved dog-like skills for interpreting human social behaviors as a result of their domestication but also that such behaviors can arise simply as an incidental byproduct of selection for reduced reactivity to humans (Hare et al 2002, Hare et al 2005). This implies that domestic dogs’ abilities to follow human signals may have originated in a similar manner, as a byproduct of selection on tame behavior. While there is evidence to suggest that cue-following skills arose as a byproduct of selection on emotional reactivity (Hare and Tomasello 2005), it is currently unclear whether additional selection in dogs produced alterations in these abilities according to different breeding criteria. Numerous behavioral differences exist among dog breeds, from distinctions in problem-solving behavior to more general traits such as aggressiveness and reactivity (Christiansen et al 2001, Scott and Fuller 1965, Wilsson and Sundgren 1997). However, a recent paper did not find differences between breeds in a human-focused social behavior, detour-following ability (Pongracz et al 2005). As such, dog breeds may not differ in their abilities to follow human cues to hidden food. It is possible that regardless of breeding criteria, close human interaction has produced increased sensitivity to human cues equally in all breeds. Alternatively, one might expect that breeds selected to interact frequently in a communicative context with humans, such as retrievers or shepherds, should use human signals more skillfully than other breeds. No controlled experiment has yet been performed to test this hypothesis. The present experiments were designed to distinguish whether there are in fact differences between breeds in their cue-following abilities.

208 Victoria Wobber et al.

In our first experiment, we investigated the cue-following abilities of New Guinea Singing Dogs (NGSDs), a group of dogs thought never to have been bred for their ability to use human signals in any context. In fact, it is suspected that NGSDs, a close relative of the Australian dingo, have had little contact with humans for over 5,000 years (Koler-Matznick 2002, Koler-Matznick et al 2003, Vila et al 1997). By comparing NGSDs to a cross-section of breeds representing those which have lived in contact with humans in recent history, we were able to discriminate whether general exposure to humans has caused changes in cue-following ability relative to a breed which has had very little interaction with humans. If this general exposure were not important, with dogs’ cue-following abilities instead being determined by early selection on emotional reactivity and not altered thereafter, then the NGSDs and the other dog breeds should show similar abilities to follow human cues. In the second experiment, we aimed to determine whether there are distinctions in cue-following among breeds that have had similar degrees of contact with humans. We investigated two potential hypotheses that might explain changes in cue-following performance. First, we asked whether dogs selected to interact in communicative contexts with humans perform better in tests of cue-following than those not subject to such selection. This would be expected if communicative skill is a heritable trait that has been selected in these breeds. Alternatively, since certain breeds of dog have been demonstrated to be more genetically wolflike than others (Parker et al 2004), a breed’s genetic distance from wolves might explain variation in cue use. This would be expected if communicative skills were enhanced by more general selection pressures on tame behavior rather than by selection for skill in interpreting human signals. In this second experiment we used a 2x2 design to determine which hypothesis better explained variation in cue-following across breeds.

Experiment 1 In our first experiment we compared the cue-following abilities of a group of dogs belonging to various breeds to that of New Guinea Singing Dogs (NGSDs). Since both groups are domesticated, we predicted that they would both show some skill at using human social cues. But, based on the difference in intensity of human involvement in their different breeding history, we predicted that the NGSDs would use cues less skillfully or in a different way relative to the other dogs.


Method Subjects Eighteen dogs from nine different breeds (mean age of 4.6 years with 4 females and 14 males) and nine New Guinea Singing Dogs (mean age of 4.7 years with 5 females and 4 males) participated in this experiment. Individuals were from the following breeds: 6 golden retrievers, 3 labrador retrievers, 3 dalmatians, 2 German shepherds, 1 Bernese mountain dog, 1 Irish setter, 1 hovawart, and 1 German pinscher. Though most of these are considered to be working dogs by major kennel clubs, some are also ‘companion’ breeds. We used a mix of breeds to represent the average performance of working and companion dogs, rather than singling out any one breed to compare to the NGSDs. The pedigree of the subjects in the working/companion dog group was assured by verifying that the subjects’ parents were pure-bred (i.e. registered with a kennel club). All dogs were raised as family pets and were from Leipzig, Germany. All but one of the NGSDs were raised by the third author (J.M.-K.) at the New Guinea Singing Dog Conservation Society in Central Point, Oregon where they are housed together. The ninth was tested at its owner’s home. NGSDs were only recently described. They represent an ancient lineage closely related to Australian dingos and show characteristic signs of domestication (e.g. dog-like forms of tame behavior toward humans as adults, etc.). However, few, if any, NGSDs are kept as pets in New Guinea or elsewhere and it is believed that these dogs have lived virtually free of human contact for thousands of years (Koler-Matznick 2002, Koler-Matznick et al 2003). All of the NGSDs in the current study were raised largely in the same way one would raise a pet dog. They were frequently held and played with as puppies and have lived in close contact with humans and other dogs during their adult life. To ensure that subjects maintained motivation throughout testing owners were asked not to feed their dogs on the morning that they were tested. During testing water was always available to all subjects ad libitum. Set-up The NGSDs were tested in a familiar enclosure of their outdoor kennel. The working/companion dogs were tested in a novel room at the Max Planck Institute dog testing facility. Two bowls (16 cm diameter, 8 cm high) were placed on the ground 1.2 meters apart. One experimenter (E1) sat behind the bowls and across from the subject who was held on a leash by another experimenter (E2) at the starting point which was 1.5 meters from each of the bowls (Figure 1).


Figure 1. Test setup. The experimenter sat equidistant between the two bowls, 1.5 meters from where the dog sat at a pre-determined point (delineated by the tape markings on the floor). Here, the experimenter is giving the Gaze cue (Experiment 2).

Procedure In order to introduce each subject to the test situation E1 showed the subject a piece of food while E2 held the subject at the starting point. Once E1 had the subject’s attention (sometimes this required calling the subject’s name), E1 would then place the food into one of the two bowls as the subject watched. After a bowl was baited the subject was released by E2 and allowed to approach one of the bowls. If they touched the baited bowl first they were allowed to retrieve and eat the food, while if they chose the empty bowl first they were shown where the food was hidden but not allowed to eat the food. If subjects retrieved food in 13 or more of 18 of these pre-test trials, they moved on to the test conditions. The test procedure was identical to that of the introduction with the exception that once E1 captured the attention of the subject E1 sham-baited one of the bowls while hiding the food in the other (or vice versa) — so that subjects knew the food was hidden but did not know where. Bowls were always baited in full view of the subjects, both in test and control conditions, as performed in previous studies of this type (Agnetta et al 2000, Hare et al 1998). Once the bowl was baited and the subject was attentive, E1 gave one of three social cues to communicate the location of the hidden food.


Point and Gaze. E1 extended her cross-lateral arm and index finger (approximately 50 cm from the bowl) toward the baited bowl while turning her head and eyes to look in the direction of the bowl. Block. E1 showed the subject a small wooden block (8 cm³) by shaking it rapidly and then placed it in front of the baited bowl as the subject watched. E1 then took her original position and stared straight ahead. Static block. E1 showed the subject the same block as used in the previous condition, then the subject’s eyes were covered while E1 placed the block silently in front of the baited bowl. E1 then returned to her original position and the subject’s eyes were uncovered. Thus the subject could use the block in front of the correct bowl as a cue, but never saw the block moving toward the baited bowl. All of the visual cues were available until the subject chose one of the bowls by touching it. Again, if the subject chose the correct bowl it was allowed to eat the food reward, and if it chose the incorrect bowl it was shown the location of the food but not given the food. If at any time during a test session a subject failed to touch one of the two bowls in three consecutive trials, they were given a short break and only resumed testing after they had succeeded in four consecutive pretest trials. A control condition was also run to ensure that subjects were not able to discern the location of the food from any scent or unintended experimenter cues. This control condition was run with all subjects except three of the NGSDs (time and social constraints prevented them from being tested in the control). In this condition, E1 performed the exact baiting procedure as for the test conditions (sham baiting one bowl and actually baiting the other), then returned to her original position and stared straight ahead. The subject was then released as in the other conditions.

Design Subjects received eighteen trials of each of the three communicative cues (54 test trials total) and eighteen trials of the control condition for a total of 72 trials. All subjects received the social cues in the same order: Point/Gaze, Block, Static Block, and control condition. Thus, this meant that subjects received 18 trials of Point/ Gaze, then had a small break, then continued with 18 trials of the Block cue, etc. This order was used because it was believed to be given in increasing difficulty (the Block cue being harder than the Point/Gaze, the Static Block harder than the Block, and the Control condition the hardest). The rationale for this was that this provided subjects with the most possible test experience when they received the


harder cues, so that in case there was any confusion with the paradigm this would be overcome upon receiving the more difficult cues. While effects of fatigue may have been present across the conditions, as we mentioned, our abort criteria ensured that subjects were continuing to participate and we gave subjects breaks between conditions. Further, our next experiment controlled for any potential order effects that may have been exhibited here. A bowl was never baited with the food for more than two trials in a row and the location of the food reward was counterbalanced within and across subjects. Bowls were sham baited in the same order for every trial for every subject.

Scoring and Analysis A camera was placed in the corner of the testing room so that both the experimenter and the subject were always recorded. Subjects’ choices were coded live, with a choice being scored as soon as the subject touched one of the two bowls (the distance between bowls prevented subjects from touching two bowls simultaneously). The data was analyzed in several ways: the performance of both groups with the three communicative cues and the control cue was compared to chance using a one-sample t-test. In addition, the performance of the two different groups of dogs with each of the social cues was compared using a two-way repeated measure ANOVA with breed and social cue as factors, with 2-tailed pvalues reported below except where stated otherwise. To test for learning or a loss of motivation within each of the testing sessions, the first nine and last nine trials of each test condition from each of the two test groups were compared using a paired t-test (i.e. learning would lead to more correct choices in the second half of the trials for each condition while a loss of motivation would lead to fewer correct choices). Finally, individual performance was examined by assessing whether a subject performed significantly above chance, in this case being attained if they chose the baited bowl in 13 or more of 18 trials (p